Repeated Selection of Alternatively Adapted Haplotypes Creates Sweeping Genomic Remodeling in Stickleback

Area of Science:

• Evolutionary Biology
• Population Genomics
• Ecology

Background:

• Heterogeneous genetic divergence can arise when populations adapt to different environments while maintaining gene flow.
• Understanding the timescale and genomic extent of diversification, especially in parallel evolution from standing genetic variation, is crucial.

Purpose of the Study:

• To investigate the speed and genomic scope of adaptation in threespine stickleback populations colonizing new habitats.
• To determine the role of standing genetic variation and haplotype reuse in parallel evolutionary events.

Main Methods:

• Utilized restriction site-associated DNA sequencing (RADseq) for genotyping.
• Analyzed genomic data from replicate natural populations of threespine stickleback (Gasterosteus aculeatus) in newly formed freshwater ponds and ancestral marine environments.

Main Results:

• Broad-scale genomic repatterning occurred within dozens of generations, driven by extensive standing genetic variation.
• Freshwater populations in young ponds showed divergence in the same genomic regions as much older freshwater lake populations.
• The majority of high-frequency divergent haplotypes in ponds were also found in marine populations, indicating gene flow and selection on pre-existing variation.

Conclusions:

• Rapid adaptation and genomic restructuring can occur in short evolutionary timescales (dozens of generations) in response to new environments.
• Standing genetic variation facilitates parallel evolution, with similar haplotypes being selected in replicate populations.
• Ongoing gene flow between marine and freshwater stickleback populations maintains polymorphisms that enable rapid adaptation to divergent environments.